Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes

Texto

(1)

(2)

(3) Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes João Nuno dos Reis Franco Biologia Departamento de Biologia 2017. Orientador Iacopo Bertocci, Investigador, Stazione Zoologica Anton Dohrn, Itália. Coorientador Isabel Sousa Pinto, Professor associado, Faculdade de Ciências da U.Porto.

(4)

(5) FCUP | I Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. This thesis was supported by:. PhD grant attributed to João N. Franco SFRH/BD/84933/2012.

(6)

(7) FCUP | II Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. This thesis is based in the following articles listed below, written in collaboration with co-authors. I hereby declare that I have contributed to conceiving the ideas, compiling and producing the data and analysing the data, and also declare that I have led the writing of all chapters.. João N. Franco, Thomas Wernberg, Iacopo Bertocci, Pedro Duarte, David. Jacinto,. Nuno. Vasco-Rodrigues,. Fernando. Tuya.. Herbivory drives kelp recruits into ‘hiding’ in a warm ocean climate. Marine Ecology Progress Series, 536:1-9 *Feauture Article* João N. Franco, Fernando Tuya, Iacopo Bertocci, Laura Rodríguez, Brezo Martinez, Isabel Sousa-Pinto, Francisco Arenas. The ‘golden kelp’ Laminaria ochroleuca under global change: integrating multiple eco-physiological responses with species distribution models. Journal of Ecology. (in press), DOI: 10.1111/1365-2745.12810 João N. Franco, Thomas Wernberg, Iacopo Bertocci, David Jacinto, Paulo Maranhão, Tânia Pereira, Brezo Martinez, Francisco Arenas, Isabel Sousa-Pinto, Fernando Tuya. Modulation of different kelp life stages by herbivory: compensatory growth versus population decimation. Marine Biology. Accepted João N. Franco, Thomas Wernberg, Iacopo Bertocci, David Jacinto, Jesus Troncoso, Brezo Martinez, Nuno Vasco Rodrigues, Francisco Arenas, Isabel Sousa Pinto, Fernando Tuya. Interannual variability of kelps and their consumers in Iberia (to be submitted).

(8)

(9) FCUP | III Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. ACKNOWLEDGMENTS Many people are responsible for my success in finishing the present work.. It has been a tasteful and epic journey!!!!. I’m extremely. indebted with Dr. Fernando Tuya and to Dr. Iacopo Bertocci, and with Dr. Isabel Sousa Pinto, Dr. Francisco Arenas, Dr. Thomas Wernberg and Dr. Brezo Martinez for exposing me to different views of the world of primary producers. Their enthusiasm, encouragement, advice, support and guidance have continued to this day and are greatly appreciated. I would like to thank the staff, researchers, graduate and ungraduated students and friends at CIIMAR – Porto, Laboratório de Ciências do Mar – Sines, ESTM – Peniche, IMAR – Coimbra, A Graña Marine Station – Ferrol, ECIMAT – Vigo, Svén Loven Marine Station – Kristineberg and at city of Freiria, Torres Vedras, Ericeira, Porto, Coimbra and Lisbon for their valuable help during this journey. A final special thanks to my beloved family, for believing and supporting me all the time and for being the real “foundation and meaning” of my life..

(10)

(11) FCUP | IV. SUMMARY. Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. SUMMARY Kelp are large brown macroalgae living mostly in shallow subtidal rocky habitats of temperate and arctic coastal regions. There, they are important foundation species due to their complex tri-dimensional structure and high productivity, which support a large diversity of associated organisms and provide a variety of ecosystem services of ecological and economic value. Kelp forests are naturally resilient systems. Nevertheless, they are increasingly threatened by human and natural perturbations, including climate change, coastal anthropogenic development and herbivory. In general, shifts in patterns of distribution and abundance of kelp populations can be driven by a range of top-down and bottom up processes operating at multiple scales in space and time. Populations at their distributional range edges are expected to be firstly affected. Understanding patterns of distribution of kelps and their multiple drivers acting at local and global scales is crucial for predicting their responses under scenarios of current and expected environmental variation. This scientific information is essential for effective protection and management actions of these habitat formers and of the variety.

(12) FCUP | V Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. of associated biodiversity and ecosystem goods and services that rely on them. This thesis aimed at assessing, by means o f surveys, field and laboratory experiments conducted from 2011 to 2016,. the. patterns of distribution, abundance and diversity of kelp populations in the Iberian Peninsula, and understanding how abiotic and biological factors, acting separately or in complex interactions, shape their ecological and physiological responses. In Chapter I, the interannual variability in the abundance and frequency of occurrence of subtidal kelp species and their major consumers was investigated across the north and west coast of Iberia during a six years field survey. Two perennial and three annual kelp species were recorded: Laminaria hyperborea, Laminaria ochroleuca, Saccorhiza polyschides, Phyllariopsis brevipes and Phyllariopsis purpurascens, respectively. Annual species dominated in terms of frequency (>80%), with S. polyschides being the most abundant and frequent (about 60%) of all kelps. Perennial species, however, were more abundant in the northern regions where L. ochroleuca was the most abundant kelp being sparse, or absent, in the southern regions. Consumers were more abundant in the southern, compared to the northern, regions. Herbivorous fishes, in particular, were more frequent, and about 40 times more abundant, in the southern regions, while sea-urchins were more frequent, but 6 times less abundant, in the northern regions compared to southern regions. In Chapter II, the effects of herbivory on the performance of different life stages of L. ochroleuca sporophytes were assessed through an herbivore exclusion field experiment at central Portugal. Both the abundance and survival of all life stages increased when they were. protected. from. herbivorous. fishes. and. sea. urchins.. Concomitantly, blade linear and area growth of adult kelps displayed.

(13) FCUP | VI Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. contrasting patterns, suggesting a compensatory growth mechanism suitable to buffer the negative impact of intense grazing. In Chapter III, the effects of herbivory on the distribution and abundance of kelp recruits at two regions under contrasting ocean climate (‘cool’ vs. ‘warm’, north and central Portugal, respectively) and topography (‘open reef’ vs. ‘crevices’) were examined using a tethering field experiment. Grazing assays showed about 50 times higher rates of kelp biomass consumption, mainly by fishes, and null survival of kelp recruits in the ‘warm’ compared to the ‘cool’ region. Moreover, the abundance of kelp recruits was 3.9 times greater in the ‘cool’ region, where 85% of recruits were found in ‘open reef’ habitats. In contrast, 87 % of recruits in the ‘warm’ region were restricted to ‘crevices’. In Chapter IV, using L. ochroleuca as a model species, a combination of mesocosm experiments and modelling (SDM: Species Distribution Model) was performed to examine the effects of crossed stressors, i.e. ocean temperatures and nutrient availability, on kelp physiological performance, to forecast the patterns of distribution of L. ochroleuca under climate change scenarios. Temperatures above 24.6 ºC were lethal irrespective of nutrients, while the optimal growth of juvenile sporophytes occurred between 12 °C and 18 ºC and no nutrient limitation. The SDM, where ocean temperature was the main predictor of kelp distribution consistently with temperature thresholds identified by eco-physiological responses, suggested a future expansion towards northern latitudes and a retreat from the southern limit/boundary of the current distribution of L. ochroleuca. In conclusion, the overall trend of decline of kelps in the Iberian Peninsula reported by previous studies seems to be further supported by present findings. However, the documented large interannual variability in kelps’ patterns of distribution likely due to processes, or combination of processes, which were not controlled in present. SUMMARY.

(14) FCUP | VII Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. surveys and experiments, calls for more prolonged monitoring and extended experimentation. These are essential to better quantify and separate natural variation and anthropogenic alterations, especially in a geographic area where both are strong, but data are relatively scarce.. However, present results indicate herbivory as a key. biological process regulating both the survival and performance of kelp, at least in the ‘warm’ region of the western coast of Iberia. Moreover, herbivory does not only affect the abundance of kelp recruits across latitude, but also their distribution at local scales, driving kelp recruits into ‘hiding’ in crevices under intense grazing pressure. This implies that where the recruitment success is compromised by herbivory, the persistence of kelps would depend on the availability of topographical refuges. Adding to herbivory, the expansion or retraction of L. ochroleuca along the European coast seems to be modulated mainly by temperature, although nutrient availability. would. be. key. to. maintain. optimal. physiological. performance. Identifying such an interactive effect was only possible by the complex study illustrated in Chapter IV, since it would have been necessarily overlooked using a single stressor experimental set – up. This emphasises the need for additional multiple - stressor studies, possibly extended to other species, to understand and predict responses of kelps to more and more realistic scenarios of complex environmental change. In this context, a future restriction of kelp populations to ‘pockets’ or ‘islands’ of suitable environmental variables, acting as refuges in the north western Iberia, is expected based on present data. The present thesis contributes to increase the current knowledge on distributional shifts and responses to perturbations of kelp species. This is crucial to design future studies specifically aimed at investigating how such changes may affect local patterns of associated biodiversity and abiotic and biological processes potentially having severe ecological and economic consequences..

(15) FCUP | VIII Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. RESUMO Os kelps são algas castanhas que ocorrem normalmente habitats subtidais rochosos de pouca profundidade, nas regiões costeiras temperadas e árticas. Nestas regiões são espécies “fundadoras” importantes devido à sua complexa estrutura tridimensional e alta produtividade, uma vez que suportam uma vasta diversidade de organismos associados e providenciam diversos serviços de ecossistemas de elevado valor ecológico e económico. As florestas de kelp são sistemas naturalmente resilientes. No entanto, estão cada vez mais ameaçadas por perturbações humanas e. naturais,. incluindo. alterações. climáticas,. desenvolvimento. antropogénico na zona costeira e herbivoria. Em geral, mudanças nos padrões de distribuição e abundância das populações de kelp decorrem de vários processos top-down e bottom up que operam a diferentes escalas espaciais e temporais. Estima-se que populações de kelp que ocorrem nos seus limites de distribuição sejam as primeiras a ser afetadas. A compreensão dos padrões de distribuição dos kelps e os múltiplos fatores que os influenciam, local ou globalmente, é crucial para prever as suas respostas a cenários de variação ambiental, atuais e previstos. Essas informações científicas são essenciais para uma proteção e gestão efetiva destes “construtores” de habitat e da variedade de bens e serviços de ecossistemas e biodiversidade associados que deles dependem. Esta tese teve como objetivo avaliar, através de experiências em campo e laboratório efetuadas entre 2011 e 2016, os padrões de distribuição, abundância e diversidade das populações de kelp na Península Ibérica; e compreender como diferentes fatores abióticos e biológicos, atuando separadamente ou em interações complexas,.

(16) FCUP | IX Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. moldam as respostas ecológicas e fisiológicas das populações de kelp. No Capítulo I, investigou-se a variabilidade interanual da abundância e frequência de ocorrência de espécies de kelp e os seus principais consumidores in situ ao longo da costa norte e oeste da Península Ibérica, durante seis anos. Foram registadas duas espécies perenes (Laminaria hyperborea e L. ochroleuca) e três espécies anuais (Saccorhiza polyschides, Phyllariopsis brevipes e Phyllariopsis purpurascens). As espécies anuais dominaram em termos de frequência (> 80%), tendo sido S. polyschides a mais abundante, com cerca de 60% da abundância total de todos os kelps nas zonas amostradas. As espécies perenes foram mais abundantes nas regiões a Norte, onde L. ochroleuca foi a mais abundante, sendo raras ou ausentes nas regiões Centro e Sul. Em geral, os consumidores de kelp foram mais abundantes no Centro e Sul, em comparação com as regiões do Norte. Em particular, os peixes herbívoros foram mais frequentes e cerca de 40 vezes mais abundantes nas regiões do Centro e Sul. Por outro lado, os ouriçosdo-mar foram mais frequentes, mas 6 vezes menos abundantes nas regiões do Norte em relação às regiões do Sul. No Capítulo II, avaliou-se o efeito da herbivoria na performance de diferentes fases de vida de esporófitos de L. ochroleuca, através de uma experiência de campo excluindo herbívoros. Tanto a abundância como a sobrevivência de todas as fases de vida aumentaram quando protegidas de peixes herbívoros e ouriços do mar. Simultaneamente, o crescimento (linear e área) da lâmina dos kelp adultos apresentou padrões opostos, sugerindo um mecanismo de crescimento compensatório capaz de atenuar o impacto negativo de herbivoria intensa. No Capítulo III, investigou-se o efeito da herbivoria na distribuição e abundância de juvenis de kelp em duas regiões caracterizadas pelo.

(17) FCUP | X Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. contraste do clima oceânico ("frio" /Norte versus "quente"/Centro) e topografia ("recife aberto" versus "fendas"), numa experiência de campo através de “tethering” (amarrar/ancorar juvenis de kelp ao substrato rochoso com um fio). Os resultados destes ensaios mostraram taxas 50 vezes maiores no consumo de biomassa de kelp, maioritariamente por peixes, e uma sobrevivência nula dos juvenis de kelp na região "quente" quando comparados com a região "fria". Além disso, a abundância de juvenis de kelp foi 3.9 vezes maior na região "fria", onde 85% dos juvenis foram encontrados em habitats de "recifes abertos". Em contraste, 87% dos juvenis na região "quente" restringiram-se a "fendas". No Capítulo IV, usando L. ochroleuca como espécie modelo, realizou-se uma combinação de experiências de mesocosmos com modelação (SDM: Modelos de Distribuição de Espécies) para avaliar os efeitos cruzados de fatores de stress, i.e. temperaturas e disponibilidade de nutrientes, no desempenho fisiológico dos kelp e prever os padrões de distribuição de L. ochroleuca em diferentes cenários de alterações climáticas. As temperaturas acima de 24.6 º C foram letais, independentemente dos nutrientes. O crescimento ótimo dos juvenis ocorreu entre 12 ° C e 18 ° C e sem limitação de nutrientes. No SDM o principal preditor na distribuição dos kelp foi a temperatura do oceano, em concordância com os limites de temperatura identificados nas respostas eco-fisiológicas, sugerindo uma futura expansão desta espécie para as latitudes mais a norte e uma retração do limite/fronteira sul da atual distribuição de L. ochroleuca. Em conclusão, os resultados obtidos nesta tese reforçam a tendência geral de declínio dos kelp na Península Ibérica, descrita em estudos anteriores. No entanto, a grande variabilidade interanual dos padrões de distribuição dos kelp observada, requer uma monitorização e experimentação mais prolongada, essenciais para. RESUMO.

(18) FCUP | XI Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. melhor quantificar e separar a variação natural das alterações antropogénicas, especialmente numa área geográfica onde estas podem ser intensas, mas com escassez de dados registados. Adicionalmente, os resultados indicam a herbivoria como um processo-chave biológico regulador da sobrevivência e performance dos kelp, pelo menos na região 'quente' da costa oeste da Península Ibérica. A herbivoria não só afeta latitudinalmente a abundância de juvenis de kelp, mas também a sua distribuição a uma escala espacial local, levando os juvenis de kelp a “esconderem-se” nas fendas sob herbivoria intensa. Isto implica que quando o sucesso do recrutamento é comprometido pela herbivoria, a persistência dos kelp depende da disponibilidade de refúgios topográficos. Além da herbivoria, a expansão ou retração na distribuição de L. ochroleuca parece ser modulada principalmente pela temperatura, embora a disponibilidade de nutrientes seja fundamental para manter um ótimo desempenho fisiológico. A identificação destes efeitos interativos foi apenas possível através dos resultados obtidos no complexo estudo realizado no Capítulo IV. A necessidade de estudos adicionais com múltiplos fatores de stress, e aplicados a outras espécies, foram enfatizados de modo a entender e prever as respostas de kelp em cenários cada vez mais realistas de alterações ambientais complexas. Neste contexto, e com base nos dados atuais, prevê-se uma futura retração das populações de kelp para 'bolsas' ou 'ilhas' no noroeste da Península Ibérica, que atuarão como refúgios por apresentarem condições ambientais adequadas. Esta tese contribui para aumentar o conhecimento atual dos kelp em relação a alterações na sua distribuição e as suas respostas a diferentes perturbações. Este conhecimento é essencial para dar suporte a estudos futuros orientados no sentido de investigar como estas mudanças podem afetar os padrões locais da biodiversidade associada a kelps e processos abióticos e biológicos, com potencial impacto ecológico e económico..

(19) FCUP | XII Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. CONTENTS GENERAL INTRODUCTION. 1. Kelps: global occurrence and distribution in European waters. 3. Background of Kelp ecosystems importance. 6. Climatic, Non-Climatic and Biological forces in kelp ecosystems. 10. The Iberian Peninsula and study region. 14. General aim and thesis structure. 16. References. 18. CHAPTER I. 23. Interannual variability of kelps and their consumers in Iberia. 23. Abstract. 25. Introduction. 26. Material and methods. 28. Results. 32. Discussion. 41. References. 44. CHAPTER II. 47. Modulation of different kelp life stages by herbivory: compensatory growth versus population decimation. 47. Abstract. 49. Introduction. 50. Materials and Methods. 54. Results. 59. Discussion. 65. Supplementary material. 69. References. 71.

(20) FCUP | XIII Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processe. CHAPTER III. 75. Herbivory drives kelp recruits into ‘hiding’ under a warm ocean climate. 75. Abstract. 77. Introduction. 78. Materials and methods. 82. Results. 86. Discussion. 90. References. 97. CHAPTER IV. 103. The ‘golden kelp’ Laminaria ochroleuca under global change: integrating multiple eco-physiological responses with species distribution models. 103. Abstract. 105. Introduction. 106. Material and methods. 110. Results. 117. Discussion. 122. Supplementary material. 128. References. 132. CONCLUSIONS. 139. Conclusions. 139. Future remarks. 140.

(21) GENERAL INTRODUCTION. Figure General Introduction View of seafloor at Montanha de Camões, where Laminaria ochroleuca is present. This plateau is located at 22 Km West off Cabo da Roca (45 m depth). Photograph by R. Guerra. ..

(22) FCUP | 2 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes.

(23) FCUP | 3 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. KELPS: GLOBAL OCCURRENCE AND DISTRIBUTION IN EUROPEAN WATERS Kelps are large brown algae typically belonging to the order Laminariales. Although kelps are technically restricted to this order, several species of large canopy-forming brown algae, such as those belonging. to. the. order. Tilopteridales. (split. from. the. order. Laminariales), are often referred to as kelp. Kelps largely occur in shallow subtidal (< 30 m depth) rocky habitats in most temperate and high latitude coastal areas of the world (Dayton 1985). However, under suitable conditions, such as very clear water, some species of kelp may occur at much greater depths (60 - 200 m) in other geographic areas, including tropical regions, where they are known to form extensive deep-water forests (Graham et al. 2007). Most of kelp forests are made of five dominant genera: Laminaria, Ecklonia, Lessonia, Nereocystis and Macrocystis (Fig. 1). Laminaria is the dominant genus in the eastern and western Atlantic Ocean and the. GENERAL INTRODUCTION Kelps: Global occurrence and distribution in European waters.

(24) FCUP | 4 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. western Pacific Ocean; Ecklonia is prevalent in Austral Asia and South Africa; Nereocystis is common along the Pacific coast of North America; the giant kelp Macrocystis dominates along the Pacific coasts of North and South America, Southern Australia and New Zealand (Lüning 1990; Mann 2000; Guiry and Guiry 2017). Figure 1. Geographic distribution of kelp forests in surface (blue lines) and deep (red lines) waters. Adapted from Santelices (2007). Figure 1. Geographic distribution of kelp forests in surface (blue lines) and deep (red lines) waters. Adapted from Santelices (2007). In most coastal areas of Europe, provided the suitable hard substratum (continuous rock, boulders, cobbles, artificial structures) and adequate water quality, one or more species of kelp may be found. There are 13, including two aliens, confirmed species of kelp in European waters (Table 1), eight of which are present in Iberian coastal waters (Araújo et al. 2003; Assis et al. 2009; Gallardo et al. 2016)..

(25) GENERAL INTRODUCTION Kelps: Global occurrence and distribution in European waters. FCUP | 5 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. Table 1. Kelp species (order Laminariales and Tilopteridales) and their distribution in. European. waters. (according to Lüning 1990, Guiry and Guiry 2017, and references therein).. Kelp species Alaria esculenta (Linnaeus) Greville Chorda filum (Linnaeus) Stackhouse. Distribution Spitzbergen; Murmansk to southern Brittany Spitzbergen; Novaya Zemlya to northern Spain. Laminaria digitata (Hudson) Lamouroux. Spitzbergen; Murmansk to Brittany. Laminaria hyperborea (Gunnerus) Foslie. Spitzbergen; Murmansk to northern Portugal. Laminaria japonica a Areschoug. Mediterranean. Laminaria ochroleuca Bachelot de la Pylaie. Bristol Channel - Morocco; Mediterranean. Laminaria rodriguezii Bornet. Mediterranean. Laminaria solidungula J. Agardh. Spitzbergen, Novaya Zemlya. Phyllariopsis brevipes (C. Agardh) Henry et South. Southern Bay of Biscay to Morocco; Mediterranean. Phyllariopsis purpurascens (C. Agardh) Henry et South. Northern Spain to Morocco; Mediterranean. Saccharina latissima (Linnaeus) C.E. Lane. Spitzbergen; Murmansk to northern Portugal. Saccorhiza dermatodea (de la Pylaie) J. Agardh. Spitzbergen; Novaya Zemlya to midNorway. Saccorhiza polyschides (Lightfoot) Batters. Mid-Norway to Ghana; parts of Mediterranean. Undaria pinnatifida a (Harvey) Suringar a. introduced species. Channel coasts to Portugal; Mediterranean.

(26) FCUP | 6 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. BACKGROUND OF KELP ECOSYSTEMS IMPORTANCE The majority of our planet is covered by oceans with a capacity to sustain life vastly larger than that of their terrestrial counterparts. It has been estimated that aquatic plants (sensu lato) provide roughly half of the global primary production of organic matter (Falkowski and Raven 2007). Since salty seas occupy globally much larger areas than freshwater lakes and rivers, there is no doubt that the majority of aquatic productivity relies on primary producers of the oceans, especially from coastal ecosystems (Beer et al. 2014). Indeed, kelps are among the most representative primary producers on rocky coasts of temperate regions. Due to their high productivity and complex tri-dimensional structure, kelps are important foundation species (sensu Dayton 1985) (Fig. 2)..

(27) FCUP | 7 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. GENERAL INTRODUCTION Background of kelp ecosystems importance. Figure 2. Overview above (A) and below (B) the canopy of a Saccorhiza polyschides kelp forest in the Iberian coast. Photographs by N.V. Rodrigues. Figure 2. Overview above. (A) and below (B) the canopy of a. A. Saccorhiza polyschides. kelp forest in the Iberian coast. Photographs by N.V. Rodrigues. A. B The high growth rate of kelps is responsible for the high rates of primary production recorded for kelp forests, which rank as one of the most productive ecosystems on Earth (Mann 1972, 1973; Duarte et B al. 2013). As such, they constitute the nutrient pool for the next ecosystem level, i.e. secondary producers, hence fuelling food webs (Duggins et al. 1989; Fredriksen 2003; Page et al. 2008). In fact, the large primary production generated within kelp systems can have impacts far beyond the relatively narrow coastal stretch they occupy..

(28) FCUP | 8 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. For instance, large detached pieces of kelp commonly reach, as ‘wrack’, to coastal zones, where they become food for detritivores and microbes (Lucas et al. 1981). Such a process makes kelp carbon available to coastal communities of suspension feeders, as well as to herbivores and detritivores feeding directly on kelps, eventually leading to its decomposition, recycling or export out of the system (Duggins et al. 1989; Spalding et al. 2003; Bernardino et al. 2012). Concomitantly, the export of kelp material to offshore areas can benefit benthic organisms in the deep through ‘kelp falls’ (Bernardino et al. 2012) and pelagic organisms through dissolved organic material (Abdullah and Fredriksen 2004). Terrestrial ecosystems can also benefit as kelp washes up on beaches (Bradley and Bradley 1993; Krumhansl 2012) (Fig. 3). Figure 3. Sandy beaches benefit from imported kelp wrack from the nearby kelp forest in northern Portugal. Photograph by J.N. Franco. Overall, carbon cycling in kelp forests is characterized by rapid biomass turnover that can be as high as 10 times per year (Mann 1972). Kelps. are. known. as. hotspots. of. biodiversity,. which. is. extraordinarily high in comparison with other algal communities. For example, in some kelp forests the invertebrate fauna in 1 m2 can often.

(29) FCUP | 9 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. exceed 105 individuals, and a single kelp individual can impressively host >100 different species and 8000 individual organisms (Christie et al. 2003). The tri-dimensional structure of kelp provides substrata and microhabitats for a broad spectrum of macro- and micro- fauna and flora by increasing habitat volume, heterogeneity and complexity, and through directly providing food and shelter (Steneck et al. 2002; Smale et al. 2013; Teagle et al. 2017). Moreover, kelp canopies serve as ecologically important nursery grounds (Holbrook et al. 1990; Tegner, MJ & Dayton 2000), and offer protection to several fishes, crustaceans and molluscs, including species of commercial and conservation importance (Steneck et al. 1993, 2002; Norderhaug et al. 2005; Smale et al. 2013; Bertocci et al. 2015). On a broader scale, kelps play a crucial role as biological engineers (Jones et al. 1994) due to their ability to alter the environment and resources available to other organisms. Specifically, kelp canopies affect light (Connell 2003a), sedimentation (Connell 2003b), physical abrasion (Irving and Connell 2006), flow dynamics (Eckman et al. 1989), space availability and nature (Christie et al. 2007), and food quantity and quality (Krumhansl and Scheibling 2011; Krumhansl 2012). In addition, kelp species themselves are harvested for a wide range of uses, such as for food, food additives, pharmaceutical and cosmetic applications, animal feed, and biofuel production (Smit 2003; Kim et al. 2017). Therefore, not surprisingly, large amounts of kelp are grown commercially in marine farms in many parts of the world, where they are harvested mainly for human and animal consumption (Gutierrez et al. 2006). Finally, kelp ecosystems have high recreational and social value by providing preferred spots for fishing or diving, as well as opportunities for education on environmental issues relating to the ocean and its resources. All together, the provisioning, regulatory, habitat, social and cultural services provided by kelp ecosystems are valued in the range of billions of dollars annually (Vásquez et al. 2013; Smale et al. 2013; Bennett et al. 2016).. GENERAL INTRODUCTION Background of kelp ecosystems importance.

(30) FCUP | 10 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. CLIMATIC, NON-CLIMATIC AND BIOLOGICAL FORCES IN KELP ECOSYSTEMS There is general scientific consensus that climate is rapidly changing. Although this is of increasing concern since marine ecosystems are.

(31) FCUP | 11 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. centrally important for the biology of the planet, a comprehensive understanding of how they respond to anthropogenic climate change is still poorly developed (Hoegh-Guldberg and Bruno 2010). However, modifications of ocean temperature, biogeochemistry, salinity, sea level, UV radiation and circulation patterns have all been detected within the last few decades and are expected to continue (IPCC 2007). Increases in extreme meteorological events is also expected, including intensification and rise in the frequency, intensity and temporal variance of severe storms (e.g. Wolff et al. 2016) and heat waves (Wernberg et al. 2016). Moreover, the rising of sea temperature is accompanied by changes in patterns and strength of winds and ocean currents, upwelling and associated nutrient supply, ocean stratification, sea level and rainfall dynamics. All such physical and chemical perturbations interplay to potentially impact marine organisms, including kelps, at any level of biological organization, with direct and indirect effects which can become apparent as changes in physiology (e.g. growth and reproduction rates), abundance, distribution, phenology, ontogeny and trophic interactions (Harley et al. 2006; Brierley and Kingsford 2009; Wernberg et al. 2011; Gao et al. 2012; Richardson et al. 2012). Kelps, analogously to other primary producers, are critically controlled by the physical environment, which determines how well plants can survive in a particular area. For example, temperature is one of the most important factors controlling the geographic distribution of seaweeds, so that their tolerance to high (summer maxima) and low (winter minima) temperatures generally define their biogeographical boundaries (Lüning 1984; Adey and Steneck 2001). Once these basic requirements are met, the availability of resources (e.g., light and nutrients) dictates how fast plants grow. In the absence of disturbance, these factors determine the standing biomass of actively growing vegetation, and ultimately the amount of material fixed by photosynthesis that becomes available to higher. GENERAL INTRODUCTION Climatic, non-climatic and biological forces in kelp ecosystems.

(32) FCUP | 12 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. trophic levels (Duggins et al. 1989). In parallel with this bottom-up flow of primary production driven by the abiotic environment, topdown consumptive forces operate to alter producer biomass (Terborgh and Estes 2010). Primary producers are consumed by grazers, which in turn are fed upon by their predators. When such trophic interactions are strong, the balance between predators and grazers can effectively determine the amount and type of plant biomass and resulting levels of primary production (Pace et al. 1999). However, the balance between bottom-up and top-down regulatory processes is modulated by various forms of physical and/or chemical stressors. and/or. direct. anthropogenic. disturbances,. such. as. overfishing (Tegner et al. 1996) or declining of water quality (Matsunaga et al. 1999). These factors can contribute to alter the biomass of producers and consumers to varying degrees depending on the type of disturbance and the structure of the community prior to its occurrence (White and Jentsch 2001), ultimately making kelp forest ecosystems globally and locally dependent on complex interactions of biotic, climatic and non-climatic factors. Kelp ecosystems are naturally highly variable on temporal (seasonal and interannual) and spatial scales (Gagné et al. 1982; Cavanaugh et al. 2011; Reed et al. 2011). Different processes have been indicated as responsible for such variation, including (i) environmental and biological drivers, such as currents, temperature, substrate, depth, nutrient availability, swell intensity, size of kelp patches, grazing and structure of assemblages within a given system (Dayton 1985; Dayton et al. 1992); and (ii) variation in the ability of kelp to resist to (Ghedini et al. 2015) or recover from small- and large-scale disturbances (Edwards 2004; Scheibling et al. 2013). In general, recent evidence suggests that the capacity of kelp forests to recover from disturbance may be eroding (Wernberg et al. 2010; Ling et al. 2014). Drastic declines of kelp forests up to their replacement with completely different systems have been documented in many.

(33) FCUP | 13 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. GENERAL INTRODUCTION Climatic, non-climatic and biological forces in kelp ecosystems. regions in response to a range of climatic, non-climatic and biological stressors (Steneck et al. 2002; Connell et al. 2008; Johnson et al. 2011; Bennett et al. 2015; Filbee-Dexter et al. 2016; Wernberg et al. 2016) (Fig. 4). Figure 4. Canopy-forming algae characterise most temperate coasts (e.g. L. ochroleuca kelp forests pictured on the top), but some forests have been replaced by extensive covers of turf-forming algae (e.g. Peniche coast). Photographs by T. Wernberg and J.N. Franco.

(34) FCUP | 14 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. STUDY REGION: IBERIAN PENINSULA The Iberian Peninsula is included in the marine ecoregion of South European Atlantic Shelf within the Lusitanian province (Spalding et al. 2007). This classification is based on relative homogeneity in terms of main ecosystems, organisms and environment. However, regional studies have demonstrated local discrepancies at all these.

(35) FCUP | 15 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. GENERAL INTRODUCTION Study region: Iberian Peninsula. levels, especially along the northern and western coasts of the Iberian Atlantic Peninsula. For example, differences in mean seawater temperature are observed along this region, decreasing from south to north and increasing from west to east (Lemos and Pires 2004; Gómez-Gesteira et al. 2008). In parallel, different macroalgal assemblages and/or individual species typically associated with temperature gradients can be observed from north to south along the western coast (Lima et al. 2007; Assis et al. 2009, 2016; Tuya et al. 2012) and from west to east in northern Iberia (Fernandez 2011; Borja et al. 2013; Voerman et al. 2013; Piñeiro-Corbeira et al. 2016; Assis et al. 2017). A notable case among these is the introduced kelp Undaria pinnatifida, which is found in many parts of the Iberian coast. Adding to such documented variation in abiotic and biological characteristics, further climate-related changes, such as increase of water temperature, upwelling relaxation, increase of wave heights and storminess (Lemos and Pires 2004; Borja et al. 2013; Sydeman et al. 2014), are described and predicted for the near future in this geographic area, with expected direct and/or indirect influences on ecologically relevant macroalgae and associated biodiversity. The present PhD project was carried out at five regions of the Atlantic Iberian Peninsula (Fig. 5). Observational surveys and manipulative experiments were performed across all regions or within a subset of them depending on the specific hypotheses under examination.. Figure 5. Partial view of the Atlantic Iberian Peninsula showing the five study regions of the present PhD Project.

(36) FCUP | 16 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. GENERAL AIM AND THESIS STRUCTURE As previously illustrated, ongoing and future global environmental changes may play a key role in shaping biogeographic patterns, primary productivity and biological relationships of ecologically and economically important kelp species and associated habitats. Assessing and predicting such modifications is a main topic of current ecological research, to which the present work aimed at contributing by focusing on kelp systems occurring in the Iberian Peninsula. A lack of information in this area about kelp forests is generally acknowledged. In fact, despite the unequivocal importance of Iberian kelps at all levels, only a few empirical and quantitative studies have.

(37) FCUP | 17 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. addressed their spatial and temporal variation and clarified the mechanisms underlying their dynamics and possible decline. In order to fill these gaps, a range of descriptive and manipulative approaches were adopted, including the collection and analysis of data on kelps and their main consumers (fishes and sea urchins) from surveys carried out across the Iberian Peninsula over six years to assess their interannual variation. Such data were complemented with in situ experiments aimed at exploring the effects of herbivory on kelp performance at varying life stages. Mesocosm experiments combined with modelling aimed at assessing kelp physiological limits and forecasting potential range shifts in their distribution under varying climate change scenarios. Specifically, the present thesis is framed around four chapters; the main objective of each is: Chapter 1: To document the interannual variability of kelps and their consumers in the Iberian Peninsula (manuscript to be submitted). Chapter 2: To investigate how herbivory affects the growth and survival of different life stages of kelp (paper accepted in Marine Biology). Chapter 3: To investigate how herbivory affect kelp recruits in regions under contrasting ocean climate and their small-scale distribution (paper published in Marine Ecology Progress Series 536: 1-9). Chapter 4: To assess the physiological responses of kelp (Laminaria ochroleuca) to varying temperature and nutrients and, through the combination with Species Distribution Models, to forecast its possible distributional range shifts under varying climate change scenarios (paper in press in Journal of Ecology. doi:10.1111/13652745.12810).. GENERAL INTRODUCTION General aim and thesis structure.

(38) FCUP | 18 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. REFERENCES Abdullah, M. I., and S. Fredriksen. 2004. Production, respiration and exudation of dissolved organic matter by kelp Laminaria hyperborea along the west coast of Norway. Journal of the Marine Biological Association of the UK 84:887–894. Adey, W. H., and R. S. Steneck. 2001. Thermogeography over time creates biogeographic regions: A temperature/space/time-integrated model and an abundance-weighted test for benthic marine algae. Journal of Phycology 37:677–698. Araújo, R., I. Bárbara, G. Santos, M. Rangel, and I. Sousa-Pinto. 2003. Fragmenta chorologica occidentalia. Fragmenta chorologica occidentalia, ALGAE, 8572-8640 60:409–416. Assis, J., E. Berecibar, B. Claro, F. Alberto, D. Reed, P. Raimondi, and E. A. Serrão. 2017. Major shifts at the range edge of marine forests: the combined effects of climate changes and limited dispersal. Scientific Reports 7:44348. Assis, J., A. V. Lucas, I. Bárbara, and E. Á. Serrão. 2016. Future climate change is predicted to shift long-term persistence zones in the cold-temperate kelp Laminaria hyperborea. Marine Environmental Research 113:174–182. Assis, J., D. Tavares, J. Tavares, and A. Cunha. 2009. Findkelp, a GIS-based community participation project to assess Portuguese kelp conservation status. Journal of Coastal Research 3:1469–1473. Beer, S., M. Björk, and J. Beardall. 2014. Photosynthesis in the Marine Environment. WilleyBlackwell, Oxford. Bennett, S., T. Wernberg, T. de Bettignies, G. A. Kendrick, R. J. Anderson, J. J. Bolton, K. L. Rodgers, N. T. Shears, J.-C. Leclerc, L. Lévêque, D. Davoult, and H. C. Christie. 2015. Canopy interactions and physical stress gradients in subtidal communities. Ecology Letters 18:677–686..

(39) FCUP | 19 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. Bennett, S., T. Wernberg, S. D. Connell, A. J. Hobday, C. R. Johnson, and E. S. Poloczanska. 2016. The “Great Southern Reef”: social, ecological and economic value of Australia’s neglected kelp forests. Marine and Freshwater Research 67:47. Bernardino, A. F., L. A. Levin, A. R. Thurber, and C. R. Smith. 2012. Comparative composition, diversity and trophic ecology of sediment macrofauna at vents, seeps and organic falls. PLoS ONE 7. Bertocci, I., R. Araújo, P. Oliveira, and I. Sousa-Pinto. 2015. REVIEW: Potential effects of kelp species on local fisheries. Journal of Applied Ecology 52:1216–1226. Borja, Á., A. Fontán, and I. Muxika. 2013. Interactions between climatic variables and human pressures upon a macroalgae population: Implications for management. Ocean and Coastal Management 76:85–95. Bradley, R. A., and D. W. Bradley. 1993. Wintering Shorebirds Increase after Kelp (Macrocystis) Recovery. The Condor 95:372. Brierley, A. S., and M. J. Kingsford. 2009. Impacts of Climate Change on Marine Organisms and Ecosystems. Current Biology 19:R602–R614. Cavanaugh, K. C., D. A. Siegel, D. C. Reed, and P. E. Dennison. 2011. Environmental controls of giant-kelp biomass in the Santa Barbara Channel, California. Marine Ecology Progress Series 429:1–17. Christie, H., N. M. Jørgensen, and K. M. Norderhaug. 2007. Bushy or smooth, high or low; importance of habitat architecture and vertical position for distribution of fauna on kelp. Journal of Sea Research 58:198–208. Christie, H., N. M. Jrgensen, K. M. Norderhaug, and E. Waage-Nielsen. 2003. Species distribution and habitat exploitation of fauna associated with kelp (Laminaria Hyperborea) along the Norwegian Coast. Journal of the Marine Biological Association of the UK 83:S0025315403007653. Connell, S. D. 2003a. The monopolization of understorey habitat by subtidal encrusting coralline algae: a test of the combined effects of canopy-mediated light and sedimentation. Marine Biology 142:1065–1071. Connell, S. D. 2003b. Negative effects overpower the positive of kelp to exclude invertebrates from the understorey community. Oecologia 137:97–103. Connell, S. D., B. D. Russell, D. J. Turner, S. A. Shepherd, T. Kildea, D. Miller, L. Airoldi, and A. Cheshire. 2008. Recovering a lost baseline: Missing kelp forests from a metropolitan coast. Marine Ecology Progress Series 360:63–72. Dayton, P. K. 1985. Ecology of kelp communities. Annual Review of Ecology, Evolution, and Systematics 16:215–245. Dayton, P. K., M. J. Tegner, P. E. Parnell, and P. B. Edwards. 1992. Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecological Monographs 62:421–445. Duarte, C. M., I. J. Losada, I. E. Hendriks, I. Mazarrasa, and N. Marbà. 2013. The role of coastal plant communities for climate change mitigation and adaptation. Nature Climate Change 3:961–968. Duggins, D. O., C. A. Simenstad, and J. A. Estes. 1989. Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173. Eckman, J. E., D. O. Duggins, and A. T. Sewell. 1989. Ecology of under story kelp environments. I. Effects of kelps on flow and particle transport near the bottom. Journal of Experimental Marine Biology and Ecology 129:173–187. Edwards, M. S. 2004. Estimating scale-dependency in disturbance impacts: El Niños and giant kelp forests in the northeast Pacific. Oecologia 138:436–447. Ed Falkowski, P. G., and J. A. Raven. 2007. Aquatic Photosynthesis. Page Princeton University Press Published. Princeton University Press, New Jersey. Fernandez, C. 2011. The retreat of large brown seaweeds on the north coast of Spain: the case of Saccorhiza polyschides. European Journal of Phycology 46:352–360.. GENERAL INTRODUCTION References.

(40) FCUP | 20 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. Filbee-Dexter, K., C. Feehan, and R. Scheibling. 2016. Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Marine Ecology Progress Series 543:141–152. Fredriksen, S. 2003. Food web studies in a Norwegian kelp forest based on stable isotope (δ13C and δ15N) analysis. Marine Ecology Progress Series 260:71–81. Gagné, J. A., K. H. Mann, and A. R. O. Chapman. 1982. Seasonal patterns of growth and storage in Laminaria longicruris in relation to different patterns of availability of nitrogen in the water. Marine Biology 69:91–101. Gallardo, T., I. Bárbara, Afonso-CarrilloJ., B. R., M. Altamirano, A. Gómez Garreta, B. M. C. Martí, J. Rull Lluch, E. Ballesteros, and J. De la Rosa. 2016. A new checklist of benthic marinealgae of Spain. Algas. Boletín Informativo de la Sociedad Española de Ficología 51:7– 52. Gao, X., H. Endo, K. Taniguchi, and Y. Agatsuma. 2012. Combined effects of seawater temperature and nutrient condition on growth and survival of juvenile sporophytes of the kelp Undaria pinnatifida (Laminariales; Phaeophyta) cultivated in northern Honshu, Japan. Journal of Applied Phycology 25:269–275. Ghedini, G., B. D. Russell, and S. D. Connell. 2015. Trophic compensation reinforces resistance: Herbivory absorbs the increasing effects of multiple disturbances. Ecology Letters 18:182–187. Gómez-Gesteira, M., M. DeCastro, I. Alvarez, and J. L. Gómez-Gesteira. 2008. Coastal sea surface temperature warming trend along the continental part of the Atlantic Arc (1985–2005). Journal of Geophysical Research 113:C04010. Graham, M. H., B. P. Kinlan, L. D. Druehl, L. E. Garske, and S. Banks. 2007. Deep-water kelp refugia as potential hotspots of tropical marine diversity and productivity. Proceedings of the National Academy of Sciences 104:16576–16580. Guiry, M. D., and G. M. Guiry. 2017. AlgaeBase. World-wide electronic publication, National University of Ireland. Gutierrez, A., T. Correa, V. Muñoz, A. Santibañez, R. Marcos, C. Cáceres, and A. H. Buschmann. 2006. Farming of the giant kelp Macrocystis pyrifera in southern Chile for development of novel food products. Journal of Applied Phycology 18:259–267. Harley, C. D. G., a Randall Hughes, K. M. Hultgren, B. G. Miner, C. J. B. Sorte, C. S. Thornber, L. F. Rodriguez, L. Tomanek, and S. L. Williams. 2006. The impacts of climate change in coastal marine systems. Ecology letters 9:228–41. Hoegh-Guldberg, O., and J. F. Bruno. 2010. The Impact of Climate Change on the World’s Marine Ecosystems. Science 328:1523–1528. Holbrook, S. J., M. H. Carr, R. J. Schmitt, and J. A. Coyer. 1990. Effect of giant kelp on local abundance of reef fishes: the importance of ontogenetic resource requirements. IPCC.2007. (n.d.). Climate Change 2007, Synthesis Report. A Contribution of Working Groups I, II, and III to the Third Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK. Irving, A. D., and S. D. Connell. 2006. Physical disturbance by kelp abrades erect algae from the understorey. Marine Ecology Progress Series 324:127–137. Johnson, C. R., S. C. Banks, N. S. Barrett, F. Cazassus, P. K. Dunstan, G. J. Edgar, S. D. Frusher, C. Gardner, M. Haddon, F. Helidoniotis, K. L. Hill, N. J. Holbrook, G. W. Hosie, P. R. Last, S. D. Ling, J. Melbourne-Thomas, K. Miller, G. T. Pecl, A. J. Richardson, K. R. Ridgway, S. R. Rintoul, A. Slotwinski, K. M. Swadling, and N. Taw. 2011. Climate change cascades: Shifts in oceanography, species’ ranges and subtidal marine community dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology 400:17–32. Jones, C. G., J. H. Lawton, and M. Shachak. 1994. Organisms as ecosystem Organisms engineers. Oikos 69:373–386. Kim, J. K., C. Yarish, E. K. Hwang, M. Park, and Y. Kim. 2017. Seaweed aquaculture: Cultivation technologies, challenges and its ecosystem services. Algae 32:1–13..

(41) FCUP | 21 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. Krumhansl, K. A., and R. E. Scheibling. 2011. Detrital production in Nova Scotian kelp beds: patterns and processes. Marine Ecology Progress Series 421:67–82. Lemos, R. T., and H. O. Pires. 2004. The upwelling regime off the west Portuguese coast, 1941-2000. International Journal of Climatology 24:511–524. Lima, F. P., P. A. Ribeiro, N. Queiroz, S. J. Hawkins, and A. M. Santos. 2007. Do distributional shifts of northern and southern species of algae match the warming pattern? Global Change Biology 13:2592–2604. Ling, S. D., R. E. Scheibling, A. Rassweiler, C. R. Johnson, N. Shears, S. D. Connell, A. K. Salomon, K. M. Norderhaug, A. Perez-Matus, J. C. Hernandez, S. Clemente, L. K. Blamey, B. Hereu, E. Ballesteros, E. Sala, J. Garrabou, E. Cebrian, M. Zabala, D. Fujita, and L. E. Johnson. 2014. Global regime shift dynamics of catastrophic sea urchin overgrazing. Philosophical Transactions of the Royal Society B: Biological Sciences 370:20130269– 20130269. Lucas, M. ., R. C. Newell, and B. Velimirov. 1981. Heterotrophic Utilisation of Mucilage Released During Fragmentation of Kelp (Ecklonia maxima and Laminana pallida). I. Development of Microbial Communities Associated with the Degradation of Kelp Mucilage. Marine Ecology Progress Series 4:43–55. Lüning, K. 1984. Temperature tolerance and biogeography of seaweeds: The marine algal flora of Helgoland (North Sea) as an example. Helgoländer Meeresuntersuchungen 38:305–317. Lüning, K. 1990. Seaweeds: Their Environment, Biogeography, and Ecophysiology. Page The American journal of tropical medicine and hygiene. Wiley. New York. Mann, K. H. 1972. Ecological energetics of the seaweed zone in a marine bay on the Atlantic coast of Canada. II. Productivity of the seaweeds. Marine Biology 14:199–209. Mann, K. H. 1973. Seaweeds: Their Productivity and Strategy for Growth. Mann, K. H. 2000. Ecology of coastal waters. Blackwell Science, Maldin, MA. Norderhaug, K. M., H. Christie, J. H. Fosså, and S. Fredriksen. 2005. Fish–macrofauna interactions in a kelp ( Laminaria hyperborea ) forest. Journal of the Marine Biological Association of the UK 85:1279. Pace, M., J. Cole, S. Carpenter, and J. Kitchell. 1999. Trophic cascades revealed in diverse ecosystems. Trends in ecology & evolution 14:483–488. Page, H. M., D. C. Reed, M. A. Brzezinski, J. M. Melack, and J. E. Dugan. 2008. Assessing the importance of land and marine sources of organic matter to kelp forest food webs. Marine Ecology Progress Series 360:47–62. Piñeiro-Corbeira, C., R. Barreiro, and J. Cremades. 2016. Decadal changes in the distribution of common intertidal seaweeds in Galicia (NW Iberia). Marine Environmental Research 113:106–115. Reed, D. C., A. Rassweiler, M. H. Carr, K. C. Cavanaugh, D. P. Malone, and D. A. Siegel. 2011. Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92:2108–2116. Richardson, A. J., C. J. Brown, K. Brander, J. F. Bruno, L. Buckley, M. T. Burrows, C. M. Duarte, B. S. Halpern, O. Hoegh-Guldberg, J. Holding, C. V Kappel, W. Kiessling, P. J. Moore, M. I. O’Connor, J. M. Pandolfi, C. Parmesan, D. S. Schoeman, F. Schwing, W. J. Sydeman, and E. S. Poloczanska. 2012. Climate change and marine life. Biology letters 8:907–9. Santelices, B. 2007. The discovery of kelp forests in deep-water habitats of tropical regions. Proceedings of the National Academy of Sciences of the United States of America 104:19163–19164. Scheibling, R. E., C. J. Feehan, and J.-S. Lauzon-Guay. 2013. Climate Change, Disease and the Dynamics of a Kelp-Bed Ecosystem in Nova Scotia. Pages 361–387Climate Change Perspectives From the Atlantic: Past, Present and Future. Smale, D. A., M. T. Burrows, P. Moore, N. O’Connor, and S. J. Hawkins. 2013. Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective. Ecology and evolution 3:4016–38.. GENERAL INTRODUCTION References.

(42) FCUP | 22 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. Smit, A. J. 2003. Medicinal and pharmaceutical uses of seaweed natural products : a review. Journal of Applied Phycology 16:245–262. Spalding, H., M. S. Foster, and J. N. Heine. 2003. Composition, distribution, and abundance of deep-water (>30m) macroalgal in central California. Journal of Phycology 39:273–284. Spalding, M. D., H. E. Fox, G. R. Allen, N. Davidson, Z. A. Ferdaña, M. Finlayson, B. S. Halpern, M. A. Jorge, A. Lombana, S. A. Lourie, K. D. Martin, E. Mcmanus, J. Molnar, C. A. Recchia, and J. Robertson. 2007. Marine Ecoregions of the World: A Bioregionalization of Coastal and Shelf Areas. BioScience 57:573. Steneck, R., P. A. X. Bologna, and R. S. Steneck. 1993. Kelp Beds as Habitat for American Lobster Homarus Americanus Kelp beds as habitat for American lobster Homarus american us. Marine Ecology Progress Series 100:127–134. Steneck, R. S., M. H. Graham, B. J. Bourque, D. Corbett, J. M. Erlandson, J. A. Estes, and M. J. Tegner. 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environmental Conservation 29:436–459. Sydeman, W. J., M. García-Reyes, D. S. Schoeman, R. R. Rykaczewski, S. a Thompson, B. a Black, and S. J. Bograd. 2014. Climate change. Climate change and wind intensification in coastal upwelling ecosystems. Science 345:77–80. Teagle, H., S. J. Hawkins, P. J. Moore, and D. A. Smale. 2017. The role of kelp species as biogenic habitat formers in coastal marine ecosystems. Journal of Experimental Marine Biology and Ecology Special Issue. Tegner, MJ & Dayton, P. 2000. Ecosystem eﬀects of ﬁshing in kelp forest communities. ICES Journal of Marine Science 57:579–589. Tegner, M. I. A. J., P. K. Dayton, P. B. Edwakds, K. L. Riser, P. B. Edwards, and K. L. Riser. 1996. Is there evidence for long-term climatic change in southern California kelp forests? Change 37:111–126. Terborgh, J., and J. A. Estes. 2010. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. Page Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. IslandPress, Washington, DC. Tuya, F., E. Cacabelos, P. Duarte, D. Jacinto, J. Castro, T. Silva, I. Bertocci, J. Franco, F. Arenas, J. Coca, and T. Wernberg. 2012. Patterns of landscape and assemblage structure along a latitudinal gradient in ocean climate. Marine Ecology Progress Series 466:9–19. Vásquez, J., S. Zuñiga, F. Tala, N. Piaget, D. Rodríguez, and J. M. A. Vega. 2013. Economic valuation of kelp forests in northern Chile: values of goods and services of the ecosystem. Journal of Applied Phycology 26:1–8. Voerman, S. E., E. Llera, and J. M. Rico. 2013. Climate driven changes in subtidal kelp forest communities in NW Spain. Marine environmental research 90:119–27. Wernberg, T., S. Bennett, R. C. Babcock, T. de Bettignies, K. Cure, M. Depczynski, F. Dufois, J. Fromont, C. J. Fulton, R. K. Hovey, E. S. Harvey, T. H. Holmes, G. A. Kendrick, B. Radford, J. Santana-Garcon, B. J. Saunders, D. A. Smale, M. S. Thomsen, C. A. Tuckett, F. Tuya, M. A. Vanderklift, and S. Wilson. 2016. Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172. Wernberg, T., B. D. Russell, M. S. Thomsen, C. F. D. Gurgel, C. J. a Bradshaw, E. S. Poloczanska, and S. D. Connell. 2011. Seaweed communities in retreat from ocean warming. Current biology : CB 21:1828–32. Wernberg, T., M. S. Thomsen, F. Tuya, G. A. Kendrick, P. A. Staehr, and B. D. Toohey. 2010. Decreasing resilience of kelp beds along a latitudinal temperature gradient: potential implications for a warmer future. Ecology Letters 13:685–694. White, P. S., and A. Jentsch. 2001. The Search for Generality in Studies of Disturbance and Ecosystem Dynamics. Pages 399–450Progress in Botany. Wolff, N. H., A. Wong, R. Vitolo, K. Stolberg, K. R. N. Anthony, and P. J. Mumby. 2016. Temporal clustering of tropical cyclones on the Great Barrier Reef and its ecological importance. Coral Reefs 35:613–623..

(43) FCUP | 23 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. CHAPTER I. INTERANNUAL VARIABILITY OF KELPS AND THEIR CONSUMERS IN IBERIA Figure Chapter I. Scientific diver folding up the belt transect after counting kelp individuals at Peniche. Photograph by N.V. Rodrigues.

(44) FCUP | 24 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. João N. Franco1,2, Thomas Wernberg3, Iacopo Bertocci1,4, David Jacinto5,. Jesus. Troncoso6,. Brezo. Martinez7,. Nuno. Vasco. Rodrigues8, Francisco Arenas1, Isabel Sousa Pinto1,2, Fernando Tuya 9 1. CIIMAR/CIMAR, Centro Interdisciplinar de Investigação Marinha e Ambiental, Terminal de Cruzeiros do Porto de Leixões, Av. General Norton de Matos s/n, 4450-208, Matosinhos, Portugal.. 2. Departamento de Biologia, Faculdade de Ciências, Universidade do Porto, Rua do Campo Alegre s/n, 4150-181 Porto, Portugal. 3. School of Plant Biology & UWA Oceans Institute (M470), University of Western Australia, Crawley WA 6009, Australia. 4. Stazione Zoologica Anton Dohrn, Villa Comunale, 80121, Naples, Italy. 5. MARE - Marine and Environmental Sciences Centre, Laboratório de Ciências do Mar, Universidade de Évora, apartado 190, 7520903 Sines, Portugal. 6. ECIMAT, Station of Marine Sciences of Toralla, Department of Ecology and Animal Biology, University of Vigo, Spain. 7. Rey Juan Carlos University, Calle Tulipán sn., 28933 Móstoles, Madrid, Spain. 8. MARE –Marine and Environmental Sciences Centre, ESTM, Instituto Politécnico de Leiria, Leiria, Portugal. 9. IU-ECOAQUA, Grupo en Biodivesidad y Conservación, Marine Sciences Faculty, Universidad de Las Palmas de Gran Canaria, 35017, Las Palmas, Canary Islands, Spain.

(45) FCUP | 25 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. CHAPTER I Interannual variability of kelps and their consumers in Iberia. ABSTRACT Kelps are foundation species in many near-shore temperate areas, where there is wide evidence that their patterns of abundance are modulated by climatic and non-climatic drivers. We analysed, between 2011 and 2016, the interannual variability of occurrence and abundance of kelp species and their major consumers (fishes and sea urchins), as well as interannual patterns of ocean climate (seawater temperature and chl a), at five regions along a seven degrees’ latitudinal gradient encompassing the north and west coast of Iberian Peninsula. Sea surface temperature showed a significant correlation with latitude (mean variation of 0.5 - 2ºC), while chl a oscillated irregularly among the studied regions. Two perennial and three annual kelp species were recorded: Laminaria hyperborea, L. ochroleuca, Saccorhiza polyschides, Phyllariopsis brevipes and Phyllariopsis purpurascens, respectively. Kelp spatial and temporal variation were species-dependent, but annual species dominated in terms of frequency of occurrence (>80%). Saccorhiza polyschides was the most abundant species, representing ca. 60%. of total. abundance of kelps. Perennial species were relatively more abundant in the northern regions and sparse, or absent, in the southern regions. Laminaria ochroleuca was (ca. 2 times) the most abundant perennial species. Consumers were more abundant in the southern, compared to the northern, regions. Herbivorous fishes were more frequent in the southern regions and about 40 times more abundant there compared to the northern regions. Conversely, the frequency of occurrence of sea-urchins in the northern regions was lager compared to herbivorous fishes, but in the southern regions sea urchins were 6 times more abundant. The large variability of. KEYWORDS. abundance of these habitat-formers reinforce the need of adequate. abundance; Atlantic Ocean;. monitoring programs to properly assess the apparently decline of kelps particularly in regions where is recognized the lack of data, such as in the Iberian Peninsula subtidal coast.. fishes; grazers; Iberian Peninsula; Laminariales; latitude; macroecology; rocky reefs; urchins.

(46) FCUP | 26 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. INTRODUCTION Kelps are large brown macroalgae occurring along most coldtemperate rocky marine coasts and have a widely recognized ecological importance as foundation species, providing food and shelter for many organisms (reviewed by Wiencke and Bischof 2012; Ólafsson 2015; Schiel and Foster 2015). Kelp systems are highly dynamic and their spatial and temporal patterns are generally driven by the biology of the main constituent species (Dayton et al. 1992). As other primary producers, abiotic variables such as temperature and/or nutrients (Bartsch et al. 2008), and biological interactions such as herbivory (Poore et al. 2012), play a crucial rolein shaping population dynamics by affecting the physical structure, reproduction and productivity of kelps. A total of 13 kelp species are described for European coastal waters. These belong to the orders Laminariales and Tilopteridales.

(47) FCUP | 27 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. and show patterns of distribution typically related to their specific temperature tolerance (Lüning 1990). Along the Atlantic coast of southern Europe, seven kelp species are recorded (Bárbara et al. 2005; Assis et al. 2009), including the introduced Undaria pinnatifida. These species are morphologically distinct and show different growth strategies, i.e. annual (e.g. Saccorhiza polyschides, Phyllariopsis brevipes) and perennial (e.g. Laminaria ochroleuca, Laminaria hyperborea). In general, annuals are normally characterized by rapid nutrient uptake, fast growth and low nutrient storage capabilities, which make them being often considered as opportunistic species (Littler and Arnold 1980). On the contrary, perennials tend to grow slowly and to store large quantities of nutrients that can provide a sort of reserve during periods of nutrient shortage (Carpenter 1990). In the Iberian Peninsula, both types of kelp co-occur; interannual variability is expected depending on the species and the surrounding habitat. Indeed, the causes for shifts in the abundance and distribution of kelps in Europe are reported as being species-dependent and regionally variable (Araújo et al. 2016; Krumhansl et al. 2016). It is recognized, however, that the general paucity of quantitative data from many European coasts, especially in subtidal rocky reef habitats, may prevent detecting crucial ecological changes at relevant spatial scales (Smale et al. 2013). This is particularly evident for the southern Atlantic European coasts (Araújo et al. 2016). Nevertheless, recent studies have shown a declining trend of kelps in different regions along the Iberian Peninsula associated with seawater temperature increase (Fernández 2011, 2016; Assis et al. 2013; Voerman et al. 2013) and high herbivory (Franco et al. 2015). The present study was aimed at describing inter-annual patterns in the abundance of kelp species and their major consumers, i.e. herbivorous reef fishes and sea urchins, at five regions along a 7° latitudinal gradient in the northern and western coast of the Iberian Peninsula.. CHAPTER I Interannual variability of kelps and their consumers in Iberia.

(48) FCUP | 28 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. MATERIALS AND METHODS STUDY REGIONS This study was conducted at five regions in the north-western part of the Iberian Peninsula, from Galicia in Spain to the Portuguese Atlantic coast along the southern European coastline (Fig.1). The regions were Sines (SIN), Peniche (PEN), Viana do Castelo (VIA), Vigo (VIG) and Coruña (COR), each including a stretch of coast between 10 and 20 km long. The Portuguese Atlantic coastline is rectilinearly oriented from north to south, with a similar overall exposure to dominant NW.

(49) FCUP | 29 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. CHAPTER I Interannual variability of kelps and their consumers in Iberia. and W swells among regions. The shore is characterized by extensive sandy beaches interspersed with limestone, sandstone, shale or granitic reefs in both the intertidal and the shallow subtidal zone (Tuya et al. 2012). The Galician coastline is extremely rugged with open coast sections interrupted by sheltered “rías” i.e. coastal inlets formed by a partial submergence of an unglaciated river valley, and an alternation of hard substrata and sandy beaches (Bárbara et al. 2005; Piñeiro-Corbeira et al. 2016). The annual sampling in the Portuguese and the Galician regions started in 2011 and 2014, respectively, and finished at all regions in 2016.. Figure 1. Map of Iberian Peninsula showing the location of the 5 study regions: COR = Coruña (43.2° N ), VIG = Vigo (42.8° N), VIA = Viana do Castelo (41.5° N), PEN = Peniche (39.2° N) and SIN = Sines (37.8° N)..

(50) FCUP | 30 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. COLLECTION OF DATA ON OCEAN CLIMATE Sea surface temperature (SST) and chlorophyll (chl a) concentration were extracted, throughout 2011 to 2016, from monthly Level-3 Standard Mapped Image files generated by the [MODIS-Aqua] sensor available from NASA Earth observation satellites through the Interactive. Online. Visualization. and. Analysis. Infrastructure. (http://giovanni.gsfc.nasa.gov/) (Acker and Leptoukh 2007). Data were extracted from pixels that encompassed all reefs within each study region from monthly images produced from January of 2011 to December 2016.. COLLECTION OF DATA ON KELP ABUNDANCE Within each region, five rocky reefs, 1 to 5 km apart, at 6 to 11 m depth, were selected randomly. All sampling was done annually during summer months (June -July). At each reef within each region, the abundance of kelp species was estimated along five 25 × 2 m haphazardly located belt transects. All individuals of each kelp species were counted along each transect by SCUBA divers. Densities of each kelp species were expressed as the number of individuals per 50 m2. Pooled annual and perennial kelp species were expressed as frequency of occurrence over the total abundance of kelps from each region per year.. COLLECTION OF DATA ON GRAZERS ABUNDANCE At the same reefs, the number of individuals of different herbivorous fishes and sea urchins was assessed, respectively along five 25 × 4 m and five 25 × 2 m haphazardly located belt transects. Fishes were categorized according to their trophic affinities (Henriques et al. 2013; www.fishbase.org). Herbivorous fishes were considered as those able.

(51) FCUP | 31 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. to consume algae, thus also including omnivorous species (Franco et al. 2015). Densities of urchins was expressed as the number of individuals per 50 m2 and herbivorous fishes as the number of individuals per 100 m2 and as frequency of occurrence over the total abundance of grazers from each region at each sampled year.. STATISTICAL ANALYSES Pearson correlation (r) was used to describe the relationship between the mean values of oceanographic variables per region (SST and chl a) and latitude. Differences in the abundance of each kelp species, herbivorous fishes and sea urchins through the years and among regions were tested by 3-way ANOVA. Separate analyses were performed for the three Portuguese regions (SIN, PEN and VIA) sampled during the period 2011-2016 (SP1) and for all the five regions (SIN, PEN, VIA, VIG and COR) sampled during the period 2014-2016 (SP2). Therefore, the first ANOVA included the factors: Year (5 levels, random), Region (3 levels, fixed, crossed with Year), Reef (5 levels, random and nested within both Year and Region), with five transects in each reef providing the replicates. The second ANOVA bas based on the same model, but with Year and Region characterized by three and five levels, respectively. Before each ANOVA, the assumption of homogeneity of variances was checked through Cochran’s C test. Only the abundance of the herbivorous fishes and that of urchins in SP1 had to be ln(x+1)-transformed to achieve. homogeneous. variances.. When. relevant,. post-hoc. comparisons were carried out using pairwise Student-Newman-Keuls (SNK) tests (Underwood 1997).. CHAPTER I Interannual variability of kelps and their consumers in Iberia.

(52) FCUP | 32 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. RESULTS OCEAN CLIMATE CONDITIONS The five regions showed a year-round latitudinal gradient in mean SST of ~ 0.5 to 2°C (Fig. 1A, r = 0.99, n = 5, p < 0.001), but chl a did not show a significant correlation with latitude (Fig. 1B, r = 0.48, p < 0.001).. INTERANNUAL PATTERNS OF KELP ABUNDANCE Five kelp species were identified during the study, including two perennial (Laminaria hyperborea and Laminaria ochroleuca) and three annual (Saccorhiza polyschides, Phyllariopsis purpurascens and Phyllariopsis brevipes) species. However, the last two species were pooled together as Phyllariopsis spp. due to the impossibility of consistently discriminating between them underwater. Significant inter-annual and/or inter-regional variability of each kelp species was documented in the two periods (Figs. 2, 3 and Table 1)..

(53) FCUP | 33 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. CHAPTER I Interannual variability of kelps and their consumers in Iberia. Figure 1. Ocean climate patterns at 5 study regions along a latitudinal gradient in NW of Iberian Peninsula: (A) sea surface temperature (SST, n = 70 monthly values); (B) surface chl a concentration (n = 70 monthly values). COR=Coruña, VIG=Vigo, VIA=Viana do Castelo, PEN=Peniche and SIN=Sines.. INTERANNUAL PATTERNS OF KELP ABUNDANCE Five kelp species were identified during the study, including two perennial (Laminaria hyperborea and Laminaria ochroleuca) and three annual (Saccorhiza polyschides, Phyllariopsis purpurascens an.

(54) FCUP | 34 Kelps across Iberia: from patterns of abundance and distribution to top-down and bottom-up regulatory processes. Figure 2. Frequency of occurrence of kelp species pooled as perennial and annual over the total abundance of kelps (A) and herbivores (B) for each of the 5 study region through sampled years (n.a. = non available data). COR=Coruña, VIG=Vigo, VIA=Viana do Castelo, PEN=Peniche and SIN=Sines..